Temperature Stress in Advanced article

Plants . Introduction
Article Contents

Hiroomi Kai, Fukuoka Agricultural Research Center, Fukuoka, Japan . High Temperature Stress

. Genetic Engineering Approaches against High

Koh Iba, Kyushu University, Fukuoka, Japan Temperature Stress

. Chilling and Freezing Stress

. Gene Engineering Approaches against Chilling and

Freezing Stress

. Future Prospects

Online posting date: 15th April 2014

Temperature stress in plants is classified into three types temperature ranges occur depending on the altitude and
depending on the stressor, which may be high, chilling or local topography. Moreover, progressive global warming
freezing temperature. Temperature-stressed plants show may affect plants. See also: Plant Physiological Responses
low germination rates, growth retardation, reduced to Climate and Environmental Change
The development of temperature stress can be induced
photosynthesis, and often die. The elucidation of
by a high- or low-temperature, and may depend on the
mechanisms by which temperature stress causes disorders
duration of the exposure, the rate of temperature changes
is important to reveal responses by which plants cope with and the plant growth stage at which stress exposure occurs.
adverse temperature conditions. However, plants Temperature stresses are classified into high temperature
respond to temperature stress by regulating membrane (long-term exposure to 427 8C at reproductive or vegeta-
lipid composition, stress-related transcription factors, tive stage, short-term exposure to 437 8C at vegetative
metabolite synthesis and detoxification pathways. Such stage), chilling (0–15 8C) and freezing (50 8C) stresses.
plant molecular responses to temperature stress will help However, plants possess a variety of molecular mechan-
establish genetic engineering techniques to produce isms involving proteins, antioxidants, metabolites, reg-
temperature stress-tolerant plants. Genetic engineering ulatory factors, other protectants and membrane lipids
techniques have been applied to improve the adaptability to cope with temperature stress. Investigations of these
underlying molecular mechanisms lead to an under-
of plants by altering temperature stress-related gene
standing of plant adaptation to adverse temperature con-
expression in response to unfavourable temperature
ditions and will help develop temperature stress-tolerant
conditions. In this article, the authors focus on plant plants for agriculture. In this article, the focus is on the
responses and adaptation to temperature stress and negative effects of temperature stress and on the recent
strategies for the genetic improvement of temperature investigations of endogenous or engineered defence
stress tolerance in plants. mechanisms against temperature stress.

Introduction
Plants frequently are exposed to various abiotic and biotic
High Temperature Stress
stresses caused by unsuitable temperature, drought, salt,
Suppression of seed germination at supraoptimal tem-
submersion, insects, diseases, light, deficiency of nutrition,
peratures is known as thermoinhibition (Reynolds and
and so on, because plants are sessile and cannot avoid
Thompson, 1971). In lettuce, thermoinhibited seeds
adverse conditions. Temperature stress has particularly
maintained abscisic acid (ABA) contents even when the
severe effects on wild plants and commercial plant pro-
seeds were imbibed under appropriate conditions (Yosh-
duction. Temperature varies greatly, both spatially and
ioka et al., 1998). Thermoinhibition was released by exo-
temporally. In equatorial regions, daytime temperatures
genous gibberellins (GAs) (Gonai et al., 2004). ABA and
can reach 60 8C, whereas the temperature may fall
GAs are the phytohormones that regulate seed germina-
to 270 8C in winter in the polar regions. Similar
tion under high temperature stress. ABA contents in
imbibed seeds under high temperatures were increased
eLS subject area: Plant Science accompanied with upregulation of the zeaxanthin epox-
idase gene (aba1/zep) and 9-cis-epoxycarotenoid dioxy-
How to cite: genase genes (nced2, 5, 9) in Arabidopsis (Toh et al., 2008).
Kai, Hiroomi; and Iba, Koh (April 2014) Temperature Stress in Plants.
In barley seeds, pretreatment at 0 8C increased the toler-
In: eLS. John Wiley & Sons, Ltd: Chichester.
DOI: 10.1002/9780470015902.a0001320.pub2
ance against thermoinhibition during germination and
induced activities of the scavenging enzymes, superoxide

eLS & 2014, John Wiley & Sons, Ltd. www.els.net 1

 Temperature Stress in Plants

dismutase (SOD), ascorbate peroxidase (APX), catalase are produced by genetic engineering. Promising targets are
and glutathione reductase (Mei and Song, 2010). membrane lipid composition, heat shock proteins (HSPs),
Seedling exposed to temperatures above a threshold a range of proteins that act as regulatory factors, anti-
showed growth retardation, necrotic symptoms, decreased oxidants to scavenging oxygen species and other protec-
photosynthetic activity, and often died. In tobacco and tants, which are discussed in separate sections below.
Arabidopsis, O2 evolution was significantly decreased
under increasing temperature (Murakami et al., 2000). Membrane lipid composition
Tobacco seedlings developed severe necrotic symptoms
under long-term (36 8C for 60 days) and short-term (47 8C In higher plants, chloroplast membranes contain high
for 3 days) high-temperature treatments. In wheat, high amounts of trienoic fatty acids (TA), mainly 16- or 18-
temperatures increased leaf area until 10 days after anthesis carbon fatty acids with three cis double bonds. The TA
and accelerated booting, heading, anthesis and maturation level is regulated by o-3 fatty acid desaturase (FAD) cat-
(Rahman et al., 2009). However, yield components (green alysing the conversion of dienoic fatty acids including
leaf area, numbers of tillers/plant, grains/spike and weight/ hexadecadienoic (16:2) and linoleic (18:2) acids to hex-
grain) were reduced drastically so that the total grain yields adecatrienoic (16:3) and linolenic (18:3) acids in lipids. In
were lower than at appropriate temperatures. Commercial Arabidopsis thaliana, the plastid-localised FADs are the
cultivars of cyclamen (Cyclamen persicum Mill.) grown at products of fad7 and fad8 genes (Gibson et al., 1994; Iba
38 8C for 1–5 days developed browning symptoms, and et al., 1993); the endoplasmic reticulum-localised FAD is
wild-type plants cultivated at 38 8C for 14 days died at the encoded by fad3 (Arondel et al., 1992). Changes in the TA
reproductive stage (Kai et al., 2012). In wild-type cyclamen composition of chloroplast membranes are considered a
plants, amounts of some potentially cytotoxic compounds factor in the metabolic adaptation to environmental
called electrophiles increased with the occurrence of heat- stresses (Somerville and Browse, 1991). Mutants or
induced leaf damages (Kai et al., 2012). Electrophiles are genetically produced plants with decreased TA con-
derived from unsaturated fatty acids such as a-linolenic centrations in chloroplast membranes acquired thermo-
acids. Plant cells are damaged by excess levels of electro- tolerance (Figure 1a; Kai et al., 2012; Murakami et al., 2000;
philes, although lower levels can modulate the expression Routaboul et al., 2012). Therefore, decreased TA levels
of stress-related genes to avoid adverse conditions (Farmer could provide as a tool to improve thermotolerance for
and Davoine, 2007). commercial plant production. One potential mechanism
The reproductive stage is the most sensitive stage to by which reduced TA increases thermotolerance was
temperature stress, and high temperatures severely impact revealed by measurements of TA-derived compounds in
fertility. Spikelet fertility in rice was approximately 95% at transgenic cyclamen plants with decreased TA content
normal temperature (29 8C) during anthesis, but was (Kai et al., 2012). In vivo, TA peroxidation via enzymatic
reduced to 18–71%, depending on the genotype, at 38 8C and nonenzymatic pathways generates a wide variety of
(Jagadish et al., 2010). In addition, a high temperature metabolites (Esterbauer et al., 1991; Alméras et al., 2003),
during grain maturation impairs grain filling and quality in and some of them contain a, b-unsaturated carbonyl
cereals. Exposure of rice to high temperatures (day 33 8C/ groups, and are strongly cytotoxic (Esterbauer et al., 1991;
night 28) during grain development reduced the levels of Alméras et al., 2003; Mano et al., 2009). The amounts of
sugar phosphates involved in glycolysis/gluconeogenesis TA-derived acrolein (ACR) and methyl vinyl ketone
and of organic acids related to the tricarboxylic acid cycle (MVK) in wild-type cyclamen increased in parallel with the
(Yamakawa and Hakata, 2010). High temperatures might appearance of leaf damages during heat treatment (38 8C),
induce the downregulation of sucrose import/degradation whereas the amounts of both substances in transgenic
and starch biosynthesis, and the upregulation of starch cyclamen plants remained low without apparent leaf
degradation (Yamakawa and Hakata, 2010). High-tem- damages. Infiltration of leaves with ACR and MVK
perature periods after anthesis decreased the amounts of mimicking levels detected in heat-stressed wild-type plants
grain starch due to the reduction of amylopectin, and reproduced the stress symptoms. These results suggested
induced changes of starch granule size, shape and structure that thermotolerance is closely correlated with the pro-
in wheat (Liu et al., 2011). duction of toxic ACR and MVK from membrane TAs
under heat stress (Figure 1b; Kai et al., 2012). It appears
possible to produce thermotolerant plants with suppressed
expression of plastid-localised FAD, and with reduced TA
Genetic Engineering Approaches contents.
against High Temperature Stress
HSPs
To avoid negative effects of high temperature stress,
molecular approaches are being pursued to produce HSPs are molecular chaperones involved in the protection
heat stress-tolerant plants. On the basis of investigations of cells from biotic and abiotic stresses. The amino acid
of molecular mechanisms of plant responses to high tem- sequence of HSPs is well conserved in prokaryotes and
perature stress, transgenic plants with heat stress tolerance eukaryotes. In plants, HSPs are classified into five groups:

2 eLS & 2014, John Wiley & Sons, Ltd. www.els.net

 Temperature Stress in Plants

Water-infiltrated
(20 °C, 3 days)

Heat stressed
5 (38 °C, 5 days)

ACR
(20 °C, 5 ppm, 3 days)

MVK
14
(20 °C, 50 ppm, 2 days)

(Days)
Victoria T15
(a) (TA: 52%) (TA: 1.4%) (b)

Figure 1 Thermotolerant cyclamen with reduced TA-derived compounds, ACR and MVK (Kai et al., 2012). (a) Comparison of thermotolerance in the
cyclamen cultivar ‘Victoria’ and the transgenic plant (T15) with low TA contents at the reproductive stage under heat stress (38 8C, constant light). The TA
contents of leaf tissues in each plant indicate under side of the panel. Scale bar, 10 cm. (b) Damage symptoms displayed by excised cyclamen leaves after
heat stress treatment (38 8C, 5 days, constant light) or infiltration with water (water-infiltrated), ACR and MVK. The infiltrated leaves were treated with
5 ppm ACR for 3 days or 50 ppm MVK for 2 days at 20 8C under 16 h light. Scale bar, 5 cm. & Professor Koh Iba.

HSP100, HSP90, HSP70, HSP60 and HSP20 or small and C) and 14 groups (A1–A9, B1–B4 and C1). Under high
HSPs (Krishna, 2004). HSPs have a functional role in the temperature stress, active HSF trimers bind to heat shock
dissociation and degradation of protein complexes and in cis-elements harbouring palindromic nucleotide sequences
the folding and stabilisation of protein molecules. HSPs are and enhance the expression of hsp genes, leading to the
induced by transient exposure to high temperature and development of thermotolerance. The expression of
protect functional proteins. Attempts were made to hsfa1a, hsfa1b, hsfa1d and hsfa2 in Arabidopsis induced
improve thermotolerance by introducing hsp genes into other HSFs and some HSPs, and was necessary for the
recipient plants. An hsp gene from maize, designated acquisition of thermotolerance under moderately high
zmhsp16.9, driven by CaMV35S was introduced into temperature stress (Liu et al., 2011; Liu and Charng, 2013).
tobacco, generating zmhsp16.9 overexpressors exhibiting Transgenic Arabidopsis plants overexpressing hsfa2
increased seed germination rate, root length and anti- exhibited dwarf phenotypes but increased thermotolerance
oxidant enzyme activity (Sun et al., 2012). Overexpression (Ogawa et al., 2007). The products of dreb are known as
of hsp70 enhanced thermotolerance in transgenic rice and transcriptional regulators involved in responses to
suppressed programmed cell death together with decreased drought, salt and cold stress. Transgenic maize lines
amounts of reactive oxygen species (ROS) (Qi et al., 2011). overexpressing zmdreb2a exhibited tolerance to 45 8C for
Constitutive expression of hsp100 in transgenic Arabi- 1 h. These transgenic lines constitutively expressed hsp
dopsis induced tolerance to exposure to 45 8C for 2 h, under standard conditions and showed higher athsfa3
whereas cosuppression lines showed no effect. These results expression levels than the wild type after heat shock
indicated that unusual accumulations of HSPs could treatment (Qin et al., 2007). These results indicated that
improve cell viability under heat stress. regulatory factors directly or indirectly induced accumu-
lation of stress-related gene products such as HSPs under
Regulatory factors high temperature conditions and contributed to
thermotolerance.
Regulatory factors such as heat shock factors (HSFs),
dehydration response element binding proteins (DREB), Antioxidants scavenging ROS
transcription factors with WRKY domain (WRKY) and
multiprotein binding factor are involved in plant response In general, high temperature stress in plants leads to the
to a wide range of stresses. HSFs are transcriptional factors generation of various heat-inducible ROS. The moderate
that regulate the expression of hsps. In Arabidopsis, 21 accumulation of ROS plays an important role in signalling
HSF-encoding genes were classified into three classes (A, B to stress-related genes (Farmer and Davoine, 2007);

eLS & 2014, John Wiley & Sons, Ltd. www.els.net 3

 Temperature Stress in Plants

however, high ROS levels cause oxidative stress and result agents including proline, glucose, fructose, sucrose and
in cell damage (Kai et al., 2012). Several attempts were raffinose in leaves (Gilmour et al., 2004). However, freezing
made to induce thermotolerance by the introduction of stress resembles dehydration and osmotic stress with
antioxidants to scavenge harmful ROS. Transgenic Ara- respect to limitations of water transport. Furthermore,
bidopsis overexpressing barley peroxisomal apx gene tol- freezing stress resulted in ice formation in the apoplast and
erated high temperature stress (Shi et al., 2001). caused cell injuries. Arabidopsis plants exposed to freezing
Overexpression of cuznsod and apx induced thermo- stresses (from 24 8C to 210 8C for 10 h) showed reduced
tolerance to 42 8C in transgenic potato plants (Kim et al., survival rates at 6 days after the treatment (Dai et al., 2007).
2010) and transient expression of tomato phospholipid To adapt to cold conditions, plants from temperate regions
hydroperoxide glutathione peroxidase gene conferred tol- possess physiological mechanisms of cold acclimation that
erance to 55 8C for 20 min in detached tobacco leaves increase freezing tolerance by exposure to chilling tem-
(Chen et al., 2004). Antioxidants appear to decrease heat- peratures. Electrolyte leakage tests revealed that cold-
inducible ROS, contributing to improved thermotolerance acclimated Arabidopsis had a higher freezing tolerance
in transgenic plants. See also: Antioxidants than nonacclimated plants (Gilmour et al., 2004). See also:
Cold Acclimation and Freezing Tolerance in Plants
Other protectants
Under high temperature conditions, several protectants
accumulate to protect proteins and photosystems in plants. Gene Engineering Approaches
For example, exposure to high temperatures induced the against Chilling and Freezing Stress
accumulation of glycine betaine (GB), which apparently
stabilised PSII proteins (Allakhverdiev et al., 1996) in Similar to improvement of tolerance to high temperature,
many plant species. Transgenic tobacco expressing the genetic engineering can introduce chilling or freezing tol-
betaine aldehyde dehydrogenase gene from spinach accu- erance in plants.
mulated GB mainly in chloroplasts and maintained
Rubisco activity and CO2 assimilation rate under high Membrane lipid composition
temperature stress (Yang et al., 2005). Trehalose is a non-
reducing disaccharide formed from two glucose units by an TAs are the major components of chloroplast membranes.
a-1, 1-glycosidic linkage. A fusion of the yeast trehalose-6- The TA composition of chloroplast membranes varies to
phosphate synthase and trehalose-6-phosphate phospha- adapt to environmental stress (Somerville and Browse,
tase genes driven by either the constitutive CaMV35S or 1991). Increases in the TA proportion of chloroplast
the stress-regulated rd29a promoters was introduced into membranes were observed in many plant species following
alfalfa (Suárez et al., 2009). All transgenic alfalfa accu- exposure to low temperatures (Graham and Patterson,
mulated trehalose and exhibited an improved tolerance to 1982). Transgenic tobacco plants overexpressing fad7
an exposure to 45 8C for 1 h as evaluated by the survival encoding plastid-localised FAD exhibited higher TA levels
rate after 10 days. Accumulation of polyamines led to an in leaves and decreased leaf chlorosis than the wild-type
improvement of CO2 assimilation by enhancing anti- under chilling treatment at 1 8C for 7 days (Kodama et al.,
oxidant enzyme activity and protecting membrane lipids 1994). Furthermore, rice overexpressing tobacco fad3
against peroxidation (Cheng et al., 2009). encoding endoplasmic reticulum-localised FAD accumu-
lated high levels of TA in the endoplasmic reticulum of
leaves. The transgenic rice seedlings with increased TA
levels showed reduced degrees of chilling injury on leaves
Chilling and Freezing Stress on the 7th day after the end of chilling treatment at 5 8C for
9 days (Shimada et al., 2000). These results provided direct
Chilling and freezing stress results in retarded or suspended proof for an enhancement of chilling tolerance by
growth and pollen sterility. Chilling stress induced degra- increasing TA levels in plants.
dation of starch granules in mature pollen grains, inhibi-
tion of pollen germination, poor pollen tube elongation Transcription factors
and pollen sterility (Shinada et al., 2013). Chilling stress
(12 8C) increased ABA levels in spikelets of chilling-sensi- Among the various cold-signalling pathways, the C-repeat
tive rice line during 5 days chilling treatment, whereas ABA binding factor/dehydration-responsive element binding
levels of chilling-tolerant rice line increased up to 8 h but (CBF/DREB1) pathway is the best characterised one. In
subsequently they decreased to a lower level until the end of Arabidopsis, three cbf/dreb1 genes were identified that
the chilling treatment (Ji et al., 2011). Moreover, the chil- encode factors involved in the expression of cold-respon-
ling-tolerant line showed higher ABA catabolic gene sive (cor) genes (Gilmour et al., 2004). The CBF/DREB1
expression. Under chilling stress, accumulated ABA levels (mainly CBF3/DREB1) pathway is regulated by the MYC-
in rice anthers are correlated with induction of pollen type transcription factor Inducer of cbf expression 1
sterility. Arabidopsis plants exposed to chilling stress (5 8C, (ICE1), which is an upstream transcription factor reg-
7 days) increased the accumulation of cryoprotective ulating cbf genes under cold conditions. Transgenic

4 eLS & 2014, John Wiley & Sons, Ltd. www.els.net

 Temperature Stress in Plants

Arabidopsis plants overexpressing the ice1 gene induced Future Prospects

freezing tolerance (Chinnusamy et al., 2003). Moreover,
CBF3/DREB1A induced expression of cor, which Temperature stress has severe effects on all plants at seed
improved cold tolerance (Lee et al., 2005). cbf genes were germination and at the vegetative and reproductive stages.
identified not only in Arabidopsis but also in cereals Plants are not only affected by high temperature stress in
including wheat and barley. Transgenic barley plants car- progressive global warming but also by chilling and
rying tacbf14 and tacbf15 from wheat developed less severe freezing stresses because temperatures vary greatly spa-
frost-induced damages and showed increased maximum tially and temporally. Understanding plant responses and
quantum yield of photosystem II (Fv/Fm) values in the adaptation to high temperature as well as chilling and
leaves (Soltész et al., 2013). MYB transcription factors play freezing conditions is important for agricultural plant
diverse roles, for instance in responses to abiotic stress. production. Plants possess a variety of molecular
MYB proteins containing 1–3 imperfect repeats in their mechanisms involving proteins, antioxidants, metabolites,
DNA-binding domain are classified into the MYBR2R3, regulatory factors, other protectants and membrane lipids
MYBR1R2R3 and MYB-related subfamilies. Over- to cope with temperature stress. These mechanisms have
expression of osmyb2 and mybr1r2r3 induced cold-related been studied intensively in recent years. On the basis of
genes such as dreb2a and increased chilling or freezing information gained, genetic engineering approaches
tolerance (Dai et al., 2007; Yang et al., 2012). including the introduction of beneficial genes have pro-
duced temperature stress-tolerant plants. Furthermore,
temperature stress affects the regulation of the expression
Antioxidants scavenging ROS of some micro ribonucleic acids (miRNAs). These miR-
NAs are considered important regulators of functional
Oxidative stress is one of the damaging factors in plants gene expression by causing transcriptional or post-
exposed to temperature stress. Transgenic tobacco over- transcriptional gene silencing. Genome-wide association
expressing the Cu/Zn sod gene exhibited improved cold mapping is a possible method to reveal the unknown loci
tolerance (Gupta et al., 1993). The transgenic plants also that could improve temperature stress tolerance. These
showed tolerance to the superoxide-generating herbicide new approaches may reveal novel mechanisms to over-
methyl viologen. Transgenic cassava maintained higher come adverse temperature stress.
SOD and catalase levels, and showed lower mal- Despite several contributions by genetic engineering
ondialdehyde content than the wild type after cold treat- approaches to the improvement of temperature stress tol-
ment (Xu et al., 2013). In addition, tobacco overexpressing erance, problems remain in commercial plant production
the S-transferase/glutathione peroxidase gene showed and sustainable environmental safety. Transgenic plants
faster growth and higher oxidised glutathione levels than that ectopically express or constitutively overexpress tem-
wild-type plants (Roxas et al., 1997). Antioxidants perature stress-related genes exhibit unfavourable pheno-
decrease stress-inducible ROS levels, contributing to types including retarded development, slow growth and
improved tolerance to cold as well as high temperature delayed maturity compared with wild-type plants under
stress. normal growth conditions (Dai et al., 2007; Gilmour et al.,
2004; Ogawa et al., 2007; Soltész et al., 2013). One way to
solve this problem is the employment of optimised pro-
Other protectants moters to prevent the undesirable expression of stress-
related genes. In alfalfa expressing yeast genes encoding
To protect proteins and photosystems, plants accumulate trehalose-6-phoshate synthase and trehalose-6-phosphate
various protectants under temperature stress. Proline is phosphatase, biomass decreased by 21% compared with
one of the most common osmolytes accumulated under the wild type when the transgene was controlled by the
environmental stress. Proline accumulation is regulated by CaMV35S promoter, whereas it increased by 62% when
proline biosynthesis and inactivation of proline degrada- the stress-regulated rd29a promoter was used (Suárez et al.,
tion pathways. Transgenic Arabidopsis with suppressed 2009). However, there is the risk of transgene transfer to
proline dehydrogenase showed higher proline contents and other plants including weeds in the environment. The risk
exhibited freezing tolerance at 27 8C for 2 days (Nanjo can be decreased by using male-sterile plants or the appli-
et al., 1999). GB is also accumulated under environmental cation of mutagenesis rather than genetic engineering. For
stress in many plant species. Transgenic tomato produced example, changes in membrane lipid composition (TA
by introduction of the gene codA encoding a choline oxi- levels in chloroplast membranes) contribute to heat or
dase, accumulated GB and exhibited higher germination chilling tolerances. It may be possible to improve tem-
and growth rates, and tolerance to flower damages under perature stress tolerance by altering lipid composition
chilling conditions. Furthermore, the transgenic plants using mutagenesis. Further investigations into the
developed tolerance to oxidative stress induced by methyl mechanisms of plant resistance to temperature stress and
viologen (Park et al., 2004). Thus, increasing the protectant improvements of genetic engineering methodologies will
levels in plants is an effective strategy for improving chilling facilitate the production of temperature stress-tolerant
tolerance. plants.

eLS & 2014, John Wiley & Sons, Ltd. www.els.net 5

 Temperature Stress in Plants

References Ji X, Dong B, Shiran B et al. (2011) Control of abscisic acid

catabolism and abscisic acid homeostasis is important for
Allakhverdiev SI, Feyziew YM, Ahmed A et al. (1996) Stabili- reproductive stage stress tolerance in cereals. Plant Physiology
zation of oxygen evolution and primary electron transport 156: 647–662.
reactions in photosystem II against heat stress with glycinebe- Kai H, Hirashima K, Matsuda O et al. (2012) Thermotolerant
taine and sucrose. Journal of Photochemistry and Photobiology cyclamen with reduced acrolein and methyl vinyl ketone.
B: Biology 34: 149–157. Journal of Experimental Botany 63: 4143–4150.
Alméras E, Stolz S, Vollenweider S et al. (2003) Reactive elec- Kim MD, Kim YH, Kwon SY et al. (2010) Enhanced tolerance to
trophile species activate defense gene expression in Arabidopsis. methyl viologen-induced oxidative stress and high temperature
Plant Journal 34: 205–216. in transgenic potato plants overexpressing the CuZnSOD, APX
Arondel V, Lemieux B, Hwang I et al. (1992) Map-based cloning and NDPK2 genes. Physiologia Plantarum 140: 153–162.
of a gene controlling omega-3 fatty acid desaturation in Ara- Kodama H, Hamada T, Horiguchi G, Nishimura M and Iba K
bidopsis. Science 258: 1353–1355. (1994) Genetic enhancement of cold tolerance by expression of
Chen S, Vaghchhipawala Z, Li W, Asard H and Dickman MB a gene for chloroplast o-3 fatty acid desaturase in transgenic
(2004) Tomato phospholipid hydroperoxide glutathione per- tobacco. Plant Physiology 105: 601–605.
oxidase inhibits cell death induced by bax and oxidative stresses Krishna P (2004) Plant response to heat stress. Topics in Current
in yeast and plants. Plant Physiology 135: 1630–1641. Genetics 4: 73–101.
Cheng L, Zou Y, Ding S et al. (2009) Polyamine accumulation in Lee BH, Henderson DA and Zhu JK (2005) The Arabidopsis cold-
transgenic tomato enhances the tolerance to high temperature responsive transcriptome and its regulation by ICE1. Plant Cell
stress. Journal of Integrative Plant Biology 51: 489–499. 17: 3155–3175.
Chinnusamy V, Ohta M, Kanrar S et al. (2003) ICE1: a regulator Liu HC and Charng YY (2013) Common and distinct functions of
of cold-induced transcriptome and freezing tolerance in Ara- Arabidopsis class A1 and A2 heat shock factors in diverse
bidopsis. Genes & Development 17: 1043–1054. abiotic stress response and development. Plant Physiology 163:
Dai X, Xu Y, Ma Q et al. (2007) Overexpression of an R1R2R3 276–290.
MYB gene, OsMYB3R-2, increases tolerance to freezing, Liu HC, Liao HT and Charng YY (2011) The role of class A1 heat
drought, and salt stress in transgenic Arabidopsis. Plant Phy- shock factors (HSFA1s) in response to heat and other stresses in
siology 143: 1739–1751. Arabidopsis. Plant, Cell and Environment 34: 738–751.
Esterbauer H, Schaur RJ and Zollner H (1991) Chemistry and Liu P, Guo W, Jiang Z et al. (2011) Effects of high temperature
biochemistry of 4-hydroxynonenal, malondialdehyde and after anthesis on starch granules in grains of wheat (Triticum
related aldehydes. Free Radical Biology & Medicine 11: 81–128. aestivum L.). Journal of Agricultural Science 149: 159–169.
Farmer E and Davoine C (2007) Reactive electrophile species. Mano J, Miyatake F, Hiraoka E and Tamoi M (2009) Evaluation
Current Opinion in Plant Biology 10: 380–386. of the toxicity of stress-related aldehydes to photosynthesis in
Gibson S, Arondel V, Iba K and Somerville CR (1994) Cloning of a chloroplasts. Planta 230: 639–648.
temperature-regulated gene encoding a chloroplast o-3 desatur- Mei Y and Song S (2010) Response to temperature stress of
ase from Arabidopsis thaliana. Plant Physiology 106: 1615–1621. reactive oxygen species scavenging enzyme in the cross-toler-
Gilmour SJ, Fowler SG and Thomashow MF (2004) Arabidopsis ance of barley seed germination. Journal of Zhejiang University
transcriptional activators CBF1, CBF2, and CBF3 have – Science B 11: 965–972.
matching functional activities. Plant Molecular Biology 54: Murakami Y, Tsuyama M, Kobayashi Y, Kodama H and Iba K
767–781. (2000) Trienoic fatty acids and plant tolerance of high tem-
Gonai T, Kawahara S, Tougou M et al. (2004) Abscisic acid in the perature. Science 287: 476–479.
thermoinhibition of lettuce seed germination and enhancement Nanjo T, Kobayashi M, Yoshida Y et al. (1999) Antisense sup-
of its catabolism by gibberellin. Journal of Experimental Botany pression of proline degradation improves tolerance to freezing
55: 111–118. and salinity in Arabidopsis thaliana. FEBS Letters 461: 205–
Graham D and Patterson BD (1982) Response of plants to low, 210.
nonfreezing temperature: protein, metabolism, and acclima- Ogawa D, Yamaguchi K and Nishiuchi T (2007) High-level
tion. Annual Review of Plant Physiology 33: 347–372. overexpression of the Arabidopsis HsfA2 gene confers not only
Gupta S, Heinen JL, Scott Holaday A, Burke JJ and Allen RD increased thermotolerance but also salt/osmotic stress toler-
(1993) Increased resistance to oxidative stress in transgenic ance and enhanced callus growth. Journal of Experimental
plants that overexpress chloroplastic Cu/Zn superoxide dis- Botany 58: 3373–3383.
mutase. Proceeding of the National Academy of Sciences of the Park EJ, Jeknić Z, Sakamoto A et al. (2004) Genetic engineering
USA 90: 1629–1633. of glycinebetaine synthesis in tomato protects seeds, plants, and
Iba K, Gibson S, Nishiuchi T et al. (1993) A gene encoding a flowers from chilling damage. Plant Journal 40: 474–487.
chloroplast o-3 fatty acid desaturase complements alterations Qi Y, Wang H, Zou Y et al. (2011) Over-expression of mito-
in fatty acid desaturation and chloroplast copy number of the chondrial heat shock protein 70 suppresses programed cell
fad7 mutant of Arabidopsis thaliana. Journal of Biological death in rice. FEBS Letters 585: 231–239.
Chemistry 268: 24099–24105. Qin F, Kakimoto M, Sakura Y et al. (2007) Regulation and
Jagadish SVK, Muthurajan R, Oane R et al. (2010) Physiological functional analysis of ZmDREB2A in response to drought and
and proteomic approach to address heat tolerance during heat stresses in Zea mays L. Plant Journal 50: 54–69.
anthesis in rice (Oryza sativa L.). Journal of Experimental Bot- Rahman MA, Chikushi J, Yoshida S and Karim AJMS (2009)
any 61: 143–156. Growth and yield components of wheat genotypes exposed to

6 eLS & 2014, John Wiley & Sons, Ltd. www.els.net

 Temperature Stress in Plants

high temperature stress under control environment. Bangladesh cassava improves tolerance against cold and drought stresses.
Journal of Agricultural Research 34: 361–372. Plant Signaling & Behavior 8: 6.
Reynolds T and Thompson PA (1971) Characterisation of the Yamakawa H and Hakata M (2010) Atlas of rice grain filling-
high temperature inhibition of germination of lettuce (Lactuca related metabolism under high temperature: joint analysis of
sativa). Physiologia Plantarum 24: 544–547. metabolome and transcriptome demonstrated inhibition of
Routaboul JM, Skidmore C, Wallis JG and Browse J (2012) starch accumulation and induction of amino acid accumula-
Arabidopsis mutants revealed that short- and long-term ther- tion. Plant Cell Physiology 51: 795–809.
motolerance have different requirement for trienoic fatty acids. Yang A, Dai X and Zhang WH (2012) A R2R3-type MYB gene,
Journal of Experimental Botany 63: 1435–1443. OsMYB2, is involved in salt, cold, and dehydration tolerance in
Roxas VP, Smith Jr RK, Allen ER and Allen RD (1997) Over- rice. Journal of Experimental Botany 63: 2541–2556.
expression of glutathione S-transferase/glutathioneperoxidase Yang X, Liang Z and Lu C (2005) Genetic engineering of the
enhances the growth of transgenic tobacco seedlings during biosynthesis of glycinebetaine enhanced photosynthesis against
stress. Nature Biotechnology 15: 988–991. high temperature stress in transgenic tobacco plants. Plant
Shi WM, Muramoto Y, Ueda A and Takabe T (2001) Cloning of Physiology 138: 2299–2309.
peroxisomal ascorbate peroxidase gene from barley and Yoshioka T, Endo T and Satoh S (1998) Restoration of seed
enhanced thermotolerance by overexpressing in Arabidopsis germination at supraoptimal temperature by fluridone, an
thaliana. Gene 273: 23–27. inhibition of abscisic acid biosynthesis. Plant Cell Physiology
Shimada T, Wakita Y, Otani M and Iba K (2000) Modification of 39: 307–312.
fatty acid composition in rice plants by transformation with a
tobacco microsomal o-3 fatty acid desaturase gene (NtFAD3).
Plant Biotechnology 17: 43–48. Further Reading
Shinada H, Iwata N, Sato T and Fujino K (2013) Genetical and
Grover A, Mittal D, Negi M and Lavania D (2013) Generating
morphological characterization of cold tolerance at fertiliza-
high temperature tolerant transgenic plants: achievements and
tion stage in rice. Breeding Science 63: 197–204.
challenges. Plant Science 205–206: 38–47.
Soltész A, Smedley M, Vashegyi I et al. (2013) Transgenic barley
Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R and
lines prove the involvement of TaCBF14 and TaCBF15 in the
Fujita M (2013) Physiological, biochemical, and molecular
cold acclimation process and in frost tolerance. Journal of
mechanism of heat stress tolerance in plants. International
Experimental Botany 64: 1849–1862.
Journal of Molecular Science 14: 9643–9648.
Somerville CR and Browse J (1991) Plant lipid: metabolism,
Iba K (2002) Acclimative response to temperature stress in higher
mutants, and membranes. Science 252: 80–87.
plants: approaches of gene engineering for temperature toler-
Suárez R, Calderón C and Iturriaga G (2009) Enhanced tolerance
ance. Annual Review of Plant Biology 53: 225–245.
to multiple abiotic stresses in transgenic alfalfa accumulating
Miura K and Furumoto T (2013) Cold signalling and cold
trehalose. Crop Science 49: 1791–1799.
response in plants. International Journal of Molecular Science
Sun L, Liu Y, Kong X et al. (2012) ZmHSP16.9, a cytosolic class I
14: 5312–5337.
small heat shock protein in maize (Zea mays), confers heat
Sanghera GS, Wani SH, Hussain W and Singh NB (2011) Engi-
tolerance in transgenic tobacco. Plant Cell Report 31: 1473–
neering cold stress tolerance in crop plants. Current Genomics
1484.
12: 30–43.
Toh S, Imamura A, Watanabe A et al. (2008) High temperature-
Wahid A, Gelani S, Ashraf M and Foolad MR (2007) Heat tol-
induced abscisic acid biosynthesis and its role in the inhibition
erance in plants: an overview. Environmental and Experimental
of gibberellin action in Arabidopsis seeds. Plant Physiology 146:
Botany 61: 199–223.
1368–1385.
Xu J, Duan X, Yang J, Beeching JR and Zhang P (2013) Coupled
expression of Cu/Zn-superoxide dismutase and catalase in

eLS & 2014, John Wiley & Sons, Ltd. www.els.net 7